bioRxiv preprint doi: https://doi.org/10.1101/614743; this version posted April 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Phenological matching drives wheat pest range shift under climate change Yuqing Wu1,2†, Zhongjun Gong1,2†, Daniel P. Bebber3*, Jin Miao1,2†, Zhonghua Zhao4, Yuying Jiang4, Shihe Xiao5, Guoyan Zhang6, Dazhao Yu7, Jichao Fang8, Xinmin Lu9, Chaoliang Lei9, Jianqing Ding10, Qiang Wang11, Yueli Jiang1,2, Tong Li1,2, Hongmei Lian1,2, Huiling Li1,2, Yun Duan1,2, Jianrong Huang1,2, Donglin Jing12, Yunzhuan He13, Zhi Zhang14, Yunhui Zhang15, Julian Chen15, Hongbo Qiao16, Wenjiang Huang17 1Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou, 450002, CN; 2Key Laboratory of Integrated Pest Management on Crops in Southern Region of North China, Zhengzhou, 450002, CN; 3Department of Biosciences, University of Exeter, Exeter EX4 4QD, UK; 4The National Agro-Tech Extension and Service Center, Beijing, 100125, CN; 5Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 100081, CN; 6Henan Plant Protection and Plant Quarantine Station, Zhengzhou, 450002, CN; 7Hubei Academy of Agricultural Sciences, Wuhan, 430064, CN; 8Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, CN; 9Plant Sciences College, Huazhong Agricultural University, Wuhan, Hubei, CN; 430070, CN; 10Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, CN; 11Xinyang Academy of Agricultural Sciences, Xinyang, 464000, CN; 12Xingtai Institute of Agricultural Sciences, Xingtai, 054001, CN; 13College of Plant Protection, Hebei Agricultural University, Baoding, 071001, CN; 14Beijing Plant Protection Station, Beijing, 100029, CN; 15Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, CN; 16College of Information & Management Science, Hebei Agricultural University, 450002, CN; 17Institute of Remote Sensing and Digital Earth, Chinese Academy of Sciences, Beijing, 100094, CN. *Correspondence to: [email protected] † These authors contributed equally to this work. Abstract Shifting geographical ranges of crop pests and pathogens in response to climate change pose a threat to food security (1, 2). The orange wheat blossom midge (Sitodiplosis mosellana Géhin) is responsible for significant yield losses in China (3), the world’s largest wheat producer. Here we report that rising temperatures in the North China Plain have resulted in a mean northward range shift of 3.3° (58.8 km per decade) from the 1950s to 2010s, which accelerated to 91.3 km per decade after 1985 when the highly toxic pesticide hexachlorocyclohexane (HCH) was banned (4). Phenological matching between wheat midge adult emergence and wheat heading in this new expanded range has resulted in greater damage to wheat production. Around $286.5 million worth of insecticides were applied to around 19 million hectares in an attempt to minimize wheat midge damage to crops between 1985 and 2016. Despite use of these pesticides, wheat midge caused losses of greater than 0.95 million metric tons of grain during this period. Our results demonstrate the potential for indirect negative impacts of climate change on crop production and food security, and constitute the first large scale example of plant pest range shift due to global warming. 1 bioRxiv preprint doi: https://doi.org/10.1101/614743; this version posted April 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Latitudinal range shifts of wild species populations are among the strongest biological signals of recent anthropogenic climate change (5). Similar range shifts in invasive species or pests and pathogens of agricultural crops and livestock would have significant implications for biodiversity conservation or food production, respectively. While there is some evidence for latitudinal range shifts in line with global warming for crop pests and pathogens in general (1), few emerging pest outbreaks have been unequivocally attributed to climate change (2). Similarly, while many studies have modelled the effects of climatic change and variability on crop production, the impact of pests and diseases is generally ignored. Given the huge production losses attributable to crop pests and pathogens (6), and the economic and environmental burdens resulting from their control, understanding how climate change alters the risk of outbreaks is key to improving global food security in a warming world. Wheat (Triticum aestivum) is the world’s most important crop in terms of production area and second-most important in human diets. Wheat is grown mainly at temperate latitudes in both hemispheres, with China the world’s largest producer. The North China Plain (NCP, Fig. 1, Supplementary Fig. S1), comprising the provinces of Beijing, Tianjin, Hebei, Shandong, Henan, Anhui, Jiangsu, Shanghai, Zhejiang, Jiangxi and Hubei, grew around one tenth of the world’s wheat between 1961 and 2016. Orange Wheat Blossom Midge (hereafter, wheat midge), Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae) is a major wheat pest in northern latitudes around the world, including in the NCP (3). Wheat midge is univoltine and has a long diapause period during which cocooned larvae overwinter in the soil (7). Diapause is broken by winter chilling (7), followed by pupation and emergence of adults from the soil in response to warming and other climatic cues (8– 10). In North America and Europe, wheat midge larvae consume the kernels of spring wheat and other Poaceae crops, resulting in serious losses. An outbreak in northeast Saskatchewan, Canada in 1983 caused losses of $30 million across nine municipalities (11). Since this time, wheat midge has spread west and south and is now present in many regions of the Great Plains of North America (12). Adult midges are able to disperse many hundreds of kilometers on the wind (13). In China, one of the first reported 2 bioRxiv preprint doi: https://doi.org/10.1101/614743; this version posted April 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. outbreaks occurred in Wuxian, Jiangsu province in 1838 (14). By the 1950s, wheat midge had spread into the winter wheat production area in the southern region of the NCP between 28° N and 36° N (15). Henan province, for example, suffered wheat production losses of 0.352 million tons (7.7 % of production) from an outbreak in 1954 (15). The history of wheat midge outbreaks in China has been strongly influenced by the pesticide 1,2,3,4,5,6-Hexachlorocyclohexane (HCH), also called benzene hexachloride (BHC) or lindane (4). HCH was introduced as a soil treatment in the 1950s, keeping outbreaks in the NCP under control over the period 1958 to 1982 (Fig. 2). Production of HCH in China grew steadily to the mid-1970s, peaking around 250 kt before dropping to zero in 1984 (4). The NCP provinces of Jiangsu, Hunan, Henan, Shandong, Hubei, Zhejiang, Jiangxi and Hebei were among the top ten provinces with the highest HCH usage between 1952 and 1984 (4). However, serious environmental problems lead to a ban on the application of HCH in 1983 (4), resulting in the resurgence in wheat midge and a cumulative loss in wheat production of 2.77 million tons between 1985 and 2016 (Fig. 2). The resurgence of wheat midge was accompanied by a shift in the insect’s geographical range. Given predicted latitudinal range shifts under future climate change for this pest (16), and historical range shifts observed for crop pests and pathogens in general (2), the altered wheat midge distribution across the NCP over recent decades could be a result of phenological responses to climate change. Here, we investigate the pattern and causes of this range shift, testing the hypotheses that warming temperatures due to climate change allowed the insect to invade the northern regions of the NCP, and that climate change altered phenological matching that is key to successful host exploitation by the pest. Wheat midge was restricted to the southern half of the NCP in the 1950s, and the northern half in the 2010s (Fig. 1). Wheat midge damage records from 135 Counties during the period 1950 to 1959 were distributed over the provinces of Henan, Anhui, Jiangsu, Hubei, Jiangxi, Zhejiang and Shanghai across a latitudinal range of 28° N to 36° N. We term this region the Original Distribution Range (ODR). In comparison, 225 3 bioRxiv preprint doi: https://doi.org/10.1101/614743; this version posted April 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. reports of wheat midge damage in the NCP were recorded in the 2010s, across eight provinces (Hebei, Beijing, Tianjin, Shandong, Henan, Anhui, Jiangsu and Hubei) between 32° N and 40° N. Four of these provinces, Hebei, Shandong, Beijing and Tianjin, comprise a Novel Expanded Range (NER) in the northern part of the NCP that had no outbreaks during the 1950s. There were no reports of wheat midge damage in three southern provinces (Jiangxi, Zhejiang and Shanghai) below latitude 30° N in the 2010s, each of which that had recorded pest damage prior to 1960. The latitudinal median for 1950s observations was 32.74 °N (IQR 32.02 – 33.60 ° N), compared with 35.81 °N (IQR 33.81 – 37.95 °N) for the 2010s. The median latitude of midge outbreaks was 3.21 ± 0.02° SE further north in the 2010s than in the 1950s, equivalent to a range shift of 58.8 ± 0.4 km per decade (bootstrap mean of difference between median outbreak latitude in 2010s vs. 1950s). First observations of wheat midge larvae in soils at 37 sites across the NER (Supplementary Fig. S2) revealed that the insect spread northwards at a rate of 0.083 ± 0.021° N y-1, or 91.3 ± 23.3 km per decade since the resurgence of wheat midge in 1985 (Fig.